Hindawi

International Journal of Agronomy

Volume 2018, Article ID 5468602, 7 pages
https://doi.org/10.1155/2018/5468602

Research Article
Identification of Sources of Resistance for Peanut Aspergillus
flavus Colonization and Aflatoxin Contamination

Richard Moise Alansou Dieme ,1 Issa Faye,2 Yedomon Ange Bovys Zoclanclounon,3
Daniel Fonceka,3 Ousmane Ndoye,4 and Papa Madiallacke Diedhiou1
1
Université Gaston Berger, BP 211 Saint-Louis, Senegal
2
Centre National de Recherches Agronomiques de Bambey, Institut Sénégalais de Recherches Agricoles, BP 211 Bambey, Senegal
3
Centre d’Etudes Régional pour l’Amélioration de l’Adaptation à la Sécheresse, Route de Khombole, BP 3320 Thiès, Senegal
4
Conseil Ouest et centre Africain pour la Recherche et le Développement Agricoles, Avenue Bourguiba, BP 48 Dakar RP, Senegal

Correspondence should be addressed to Richard Moise Alansou Dieme; alansou7dieme@gmail.com

Received 25 May 2018; Revised 7 August 2018; Accepted 13 September 2018; Published 1 October 2018

Academic Editor: Glaciela Kaschuk

Copyright © 2018 Richard Moise Alansou Dieme et al. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
Peanut aflatoxin contamination caused by Aspergillus flavus is a serious constraint for food safety and human health in Senegal.
The present study aimed to identify sources of resistance for A. flavus colonization and aflatoxin contamination. Thus, seeds from
67 peanut genotypes were tested under laboratory conditions. Aqueous conidial suspension of an aflatoxinogenic strain of A.
flavus was used for inoculation in Petri dishes containing ten seeds of each genotype, and data on incidence and severity were
®
recorded. Total aflatoxin concentration in seeds was determined on 15th day after inoculation using mReader method. Results
showed a significant (p < 0.001) variation of aflatoxin, incidence and severity among the tested peanut genotypes. Incidence
ranged from 0 to 70% with a mean of 20.36 ± 0.8%. Out of the 67 genotypes, eight showed incidence less than 10%. Severity ranged
from 0 to 44% with a mean value of 8.82 ± 0.45%. The genotype 12CS_104 showed aflatoxin concentration level in conformity with
the European standard (4 ppb). Out of three clusters revealed by hierarchical classification based on disease incidence and severity,
the cluster 1 contained 33 genotypes characterised by low incidence and severity values. These genotypes can be tested under field
conditions to confirm their resistance to A flavus.

1. Introduction facultative plant pathogen in maize, peanut, and sesame

Peanut (Arachis hypogaea L.) is an important staple crop in
Senegal. The national peanut production was estimated at
1,050,042 tons during the rainy season of 2016 [1]. This crop
is mainly produced in Fatick, Kaolack, Kaffrine, Louga, and
Thies regions, with more than 60% of the national peanut
production [1]. Peanut seeds are widely used for food
consumption and play a significant economic role for small-
scale farmers and food industries in Senegal [2]. However,
pre- and postharvest aflatoxin contamination in peanut is
a serious threat for food safety and human health in Senegal
[3]. It is one of the major constraints limiting sustainable and
good quality seed production in the world [4]. Aflatoxin
contamination is due to Aspergillus flavus (Link ex Fries,
Teleomorph: Petromyces flavus) [5]. Damages caused by this
were reported in Senegal [6]. Considerable economic losses
caused by this bacterium are mainly due to crop quality
value and international trade restrictions on food stuffs
charged in aflatoxin [7].
Aflatoxin is the name of a group of toxin known as G1,
G2, B1, B2, M1, and M2 that produced the plant pathogen
[8]. These toxins occur naturally and have been found in
a wide range of commodities, including peanuts used for
animal and human consumption [9]. Aflatoxins are toxic,
mutagenic, and carcinogenic compounds [10]. Depending
on their levels, toxins can severely affect the liver and induce
immune-suppressing effects [9].
To handle this issue, a wide range of preharvest aflatoxin
contamination management methods were developed.
Application of atoxinogenic isolates of A. flavus [11] and
2 International Journal of Agronomy

host genetic resistance were tested [12]. In Senegal, previous Table 1: Peanut material used in this study.
studies reported that varieties 55-437 and 73-3 were resistant No Genotypes Description Country of origin
to A. flavus [13]. Identification of new sources of resistance
1 12CS_001 CSL∗ Senegal
merits to be investigated for efficient peanut breeding 2 12CS_004 CSL Senegal
program. First step of host genetic resistance is the seed 3 12CS_006 CSL Senegal
colonization test. Therefore, the present study was un- 4 12CS_007 CSL Senegal
dertaken to identify promising peanut genotypes under 5 12CS_008 CSL Senegal
laboratory conditions. 6 12CS_009 CSL Senegal
7 12CS_010 CSL Senegal
8 12CS_011 CSL Senegal
2. Materials and Methods 9 12CS_012 CSL Senegal
2.1. Plant Materials. The plant material consisted of 67 10 12CS_016 CSL Senegal
11 12CS_018 CSL Senegal
genotypes including 58 chromosomal substitutions lines
12 12CS_020 CSL Senegal
[14] and nine national released varieties. The chromosomal 13 12CS_021 CSL Senegal
substitution lines belong to a cross between Fleur 11 and 14 12CS_022 CSL Senegal
a synthetic amphidiploid parent (Table 1). 15 12CS_023 CSL Senegal
16 12CS_024 CSL Senegal
17 12CS_027 CSL Senegal
2.2. Isolation of Aspergillus flavus, Sporangial Suspension 18 12CS_028 CSL Senegal
Preparation, and Inoculation. Aflatoxinogenic strain pro- 19 12CS_031 CSL Senegal
vided from peanut seeds were purified by successive cultures 20 12CS_032 CSL Senegal
on 5/2 agar medium. The aflatoxin concentration level was 21 12CS_033 CSL Senegal
checked using the Reveal Q+ Aflatoxin test kit (accesso 22 12CS_034 CSL Senegal
®
peanut enterprise corporation, USA). The spore suspension 23 12CS_036 CSL Senegal
24 12CS_037 CSL Senegal
of A. flavus was obtained by soaking colonized seeds in 50 ml
25 12CS_039 CSL Senegal
of sterile distilled water. Then, one drop of Tween 20 was
26 12CS_041 CSL Senegal
added to the solution and thoroughly mixed for 10 minutes. 27 12CS_042 CSL Senegal
Inoculation was carried out by introducing 100 μl of the 28 12CS_047 CSL Senegal
supernatant of the spore suspension into each Petri dish. 29 12CS_048 CSL Senegal
30 12CS_050 CSL Senegal
31 12CS_051 CSL Senegal
2.3. Seed Colonization Test. The seed colonization test was 32 12CS_052 CSL Senegal
conducted following a modified Mehan and McDonald 33 12CS_053 CSL Senegal
procedure. For each genotype, 50 seeds were sterilized and 34 12CS_054 CSL Senegal
rinsed properly in sterile distilled water. Then, the seeds were 35 12CS_055 CSL Senegal
hydrated to about 20% moisture content. The 50 seeds of 36 12CS_059 CSL Senegal
each genotype were placed in 5 Petri dishes containing 10 37 12CS_060 CSL Senegal
38 12CS_061 CSL Senegal
seeds, and each Petri dish was considered as a replication.
39 12CS_062 CSL Senegal
The seeds were inoculated with a conidial suspension (60 µL 40 12CS_063 CSL Senegal
containing approximately 1 × 108 mL−1 conidia of the afla- 41 12CS_066 CSL Senegal
toxigenic strain of A. flavus). This preparation was kept at 42 12CS_070 CSL Senegal
laboratory conditions (25 ± 0.12°C and 82 ± 0.42% relative 43 12CS_072 CSL Senegal
humidity) for fifteen days. 44 12CS_075 CSL Senegal
45 12CS_076 CSL Senegal
46 12CS_078 CSL Senegal
2.4. Data Collection. The seeds’ colonization was observed 47 12CS_079 CSL Senegal
during two weeks, and aflatoxin concentration was mea- 48 12CS_084 CSL Senegal
sured using the Reveal Q+ Aflatoxin test kit (accesso peanut 49 12CS_085 CSL Senegal
®
enterprise corporation, USA). The incidence was calculated 50 12CS_090 CSL Senegal
using the following formula: 51 12CS_091 CSL Senegal
52 12CS_095 CSL Senegal
incidence(%) 54 12CS_096 CSL Senegal
55 12CS_100 CSL Senegal
number of seeds showing pathogen colonizaton 56 12CS_111 CSL Senegal
� 57 12CS_112 CSL Senegal
total number of seeds
58 12CS_118 CSL Senegal
× 100. 59 12CS_119 CSL Senegal
60 55-33 Variety Senegal
(1) 61 55-437 Resistant control Senegal
International Journal of Agronomy 3

Table 1: Continued. Table 2: Deviance values from the Poisson regression model on
incidence and severity.
No Genotypes Description Country of origin
62 73-30 CSL Senegal Source of variation Degree of freedom Incidence Severity
63 73-33 Resistant control Senegal Replication 4 33.9 (ns) 2.04 (ns)
64 78-936 Variety Senegal Genotype 66 7242.2∗∗∗ 190.08∗∗∗
65 Fleur11 Susceptible control Senegal ∗∗∗
Significant chi-squared test at 0.001 level of probability; ns � not
66 GC-8-35 Variety Senegal significant.
67 L27 Variety Senegal
∗
Chromosomal substitution lines.
presented aflatoxin concentration level up to 2000 ppb
(Figure 1).
The severity scale of aflatoxin on seeds was estimated Out of the 67 genotypes, eight showed incidence less
using a modified Tonapi et al. [15] scale. It was defined as than 10% while 33 showed incidences between 10 and 20%
follows: 0, noninfected seeds; 1, seeds whose surface covered and 16 with incidences ranged from 20 to 30% (Figure 2).
by the fungus is less than 20%; 2, 20%–40% seed surface
covered by the fungus; 3, 40%–60% seed surface covered by
the fungus; 4, 60%–80% seed surface covered by the fungus; 3.2. Correlation between Incidence, Severity, and Aflatoxin
and 5, 80%–100% seed surface covered by the fungus. The Concentration Level. Spearman’s rank correlation test
severity calculation based on Tonapi et al. [15] formula was revealed a strong relationship (r � 0.93, p < 0.001) between
as follows: incidence and severity of peanut genotypes. Positive and
significant correlations were detected between aflatoxin
􏽐ni�1 Ni × i􏼁 concentration levels and disease incidence (r � 0.28,
severity(%) � , (2)
total of seeds ×(n − 1) p < 0.01) and aflatoxin concentration levels and disease
severity (r � 0.35, p < 0.05) (Table 4).
where p < 0.001 i is severity scale from 0 to 5 and Ni is the
number of seed corresponding to scale i of severity.
3.3. Classification of the Tested Genotypes according to Sen-
sibility and Aflatoxin Concentration Level. The factorial axes
2.5. Data Analysis. Data analysis was performed with the 1 and 2 explained 60.5 and 39.5% of overall variability,
open-source statistical software R version 3.4.5 [16]. De- respectively (Figure 3). Hierarchical classification performed
scriptive statistics of recorded data were generated with on principal component analysis revealed three clusters of
pastecs package [17]. In order to find out variability of genotypes based on disease incidence and aflatoxin con-
incidence and severity according to tested genotypes, data centration levels (Figure 3). The clusters 1, 2, and 3 grouped
were subjected to Poisson regression analysis using glm 33, 20, and 14 genotypes, respectively. The incidence and
(generalized linear model) function of package stats aflatoxin concentration are significantly (p < 0.001) associ-
implemented in the R. Spearman’s rank correlation test was ated to cluster 1 (Table 4).
performed to highlight relationship between incidence, se- Mean values of these two variables in this cluster are less
verity, and aflatoxin concentration levels using correlation than the overall mean. Therefore, cluster 1 is characterized
test function of package stats. Identification of different by desirable genotypes which combine low incidence values
groups of genotypes based on incidence and severity was and aflatoxin concentration levels. Cluster 2 is significantly
performed based on a principal component analysis and (p < 0.001) related to the aflatoxin concentration level
a hierarchical clustering with the functions PCA and HCPC (Table 5).
of package FactoMineR [18], respectively. The Euclidean The mean value of aflatoxin concentration in cluster 2
distance and Ward classification method were used to (4075.5 ppb) is 190% which is higher than the overall mean
classify tested genotypes. The function fviz_pca_biplot [19] (2143.8 ppb). Thus, this second cluster is characterized by
was used to plot the principal components analysis biplot in genotypes with high level of aflatoxin. Incidence is linked to
different clusters based on hierarchical classification. cluster 3 (Table 5). Mean value of this variable (35%) in
cluster 3 is superior to overall mean (20.35%). Thus, the
3. Results cluster 3 encompasses the most susceptible genotypes to A.
flavus.
3.1. Reaction of Peanut Genotypes to Aspergillus flavus. Based on the closest distance between each genotype and
Analysis of variance revealed highly significant (p < 0.001) the respective cluster centres, 12CS_039, 12CS_010, and
variation of aflatoxin incidence and severity among the 12CS_050 were the first representative genotypes (paragon)
tested peanut genotypes (Table 2). of cluster 1, 2, and 3, respectively (Table 4). Based on the
The severity ranged between 0 and 44%, respectively, farthest distance from a genotype projected point in a cluster
with a mean of 8.82 ± 0.45%. The recorded incidence ranged to the centres of the two others, clustering revealed that
from 0 to 70% with an average value of 20.36 ± 0.80% cluster 1, 2, and 3 were characterised by the genotypes
(Table 3). 12CS_104, 78-936, and 12CS_021, respectively (Figure 3,
One genotype (12CS_104) showed aflatoxin concen- Table 5). Based on results, out of 67 genotypes, 33 promising
tration level less than 4 ppb. A total of 34 genotypes genotypes (cluster 1) were noted (Figure 3).
4 International Journal of Agronomy

Table 3: Means of incidence and severity of the tested lines. Table 3: Continued.
Incidence Severity Incidence Severity
Lines Lines
Mean Std deviation Mean Std deviation Mean Std deviation Mean Std deviation
12CS_001 44 13.42 1.02 0.44 55-33 4 5.48 0.04 0.05
12CS_004 30 12.25 0.74 0.23 55-437 12 10.95 0.18 0.19
12CS_006 30 15.81 0.46 0.29 73-30 6 5.48 0.06 0.05
12CS_007 18 8.37 0.34 0.21 73-33 16 11.40 0.28 0.19
12CS_008 12 16.43 0.22 0.27 78-936 12 4.47 0.24 0.31
12CS_009 24 8.94 0.58 0.33 Fleur_11 28 16.43 0.5 0.17
12CS_010 18 8.37 0.4 0.27 GC-8-35 22 10.95 0.6 0.24
12CS_011 18 14.83 0.42 0.48 L27 10 0.00 0.16 0.13
12CS_012 32 13.04 0.82 0.43 Mean 20.36 8.82
12CS_016 34 8.94 0.82 0.54 Standard error 0.80 0.45
12CS_018 38 13.04 0.66 0.33
12CS_020 22 10.95 0.5 0.34
12CS_021 52 10.95 1.64 0.49
12CS_022 16 15.17 0.36 0.43 Table 4: Spearman’s rank matrix correlation performed on in-
12CS_023 18 13.04 0.28 0.24 cidence, severity, and aflatoxin concentration levels data.
12CS_024 28 10.95 0.5 0.21
Aflatoxin
12CS_027 18 8.37 0.26 0.19 Incidence Severity
concentration levels
12CS_028 18 8.37 0.3 0.20
12CS_031 16 5.48 0.4 0.28 Incidence 1.00
12CS_032 14 11.40 0.16 0.11 Severity 0.93∗∗∗ 1.00
12CS_033 10 12.25 0.2 0.23 Aflatoxin ∗
0.28 0.35∗∗ 1.00
12CS_034 14 15.17 0.28 0.34 concentration levels
∗
12CS_036 14 5.48 0.26 0.15 Significant Spearman’s rank correlation test at 0.05 level of probability.
∗∗
12CS_037 16 5.48 0.32 0.19 Significant Spearman’s rank correlation test at 0.01 level of probability.
∗∗∗
12CS_039 14 8.94 0.22 0.23 Significant Spearman’s rank correlation test at 0.001 level of probability.
12CS_041 24 15.17 0.64 0.38
12CS_042 24 18.17 0.42 0.42
12CS_047 18 13.04 0.4 0.22 4. Discussion
12CS_048 6 8.94 0.08 0.13
12CS_050 34 11.40 0.76 0.29 In the present study, a wide phenotypic variation was ob-
12CS_051 34 20.74 0.72 0.36 served among the tested genotypes for incidence, severity,
12CS_052 30 15.81 0.76 0.67 and aflatoxin concentrations. This variation can be explained
12CS_053 36 15.17 0.98 0.59 by the variability of seed coat structure of the tested ge-
12CS_054 26 11.40 0.68 0.44 notypes. In fact, the seed coat can constitute a barrier to A.
12CS_055 18 8.37 0.48 0.54 flavus seed invasion depending on its thickness and/or
12CS_059 24 16.73 0.48 0.48 permeability [20], and Zhou and Liang [21] studies
12CS_060 12 13.04 0.4 0.39 showed that genotypes seed coat with smaller hilum, more
12CS_061 14 11.40 0.24 0.19
compact arrangement and thicker testa showed more re-
12CS_062 18 8.37 0.26 0.15
12CS_063 18 14.83 0.42 0.53
sistance to A. flavus. In addition, implication of wax and
12CS_066 32 22.80 0.8 0.76 cutin layers of seed coat was demonstrated to be related to
12CS_070 22 19.24 0.56 0.53 genotypes resistance [22]. Another explanation of this wide
12CS_072 14 13.42 0.26 0.28 variation in incidence, severity, and aflatoxin rate can be
12CS_075 28 13.04 0.66 0.36 biochemical compounds’ differential variability in the tested
12CS_076 12 4.47 0.18 0.08 seeds. Lindsey and Turner [23] demonstrated that the
12CS_078 10 12.25 0.16 0.18 presence of polyphenol compounds, specifically, tannins in
12CS_079 18 16.43 0.34 0.34 seed can have inhibitor effect against A. flavus. Amaya et al.
12CS_084 14 5.48 0.3 0.21 [24] and Liang et al. [25] showed the difference among seed
12CS_085 22 8.37 0.5 0.32 coat biochemical compounds to determine sensibility to A.
12CS_090 14 13.42 0.34 0.50
flavus. Liang [22] demonstrated that the presence of trypsin
12CS_091 26 11.40 0.64 0.48
12CS_095 12 8.37 0.26 0.27 in seeds can also be related to resistance to A. flavus. Turner
12CS_096 16 8.94 0.48 0.58 et al. [26] isolated and identified the 5,7-dimethoxyiso-
12CS_100 40 12.25 0.96 0.34 flavone as an inhibitor for A. flavus invasion in peanut seed.
12CS_104 6 8.94 0.14 0.26 12CS_104 was the most resistant genotype to aflatoxin
12CS_111 6 8.94 0.1 0.14 contamination with an aflatoxin level lower than the Eu-
12CS_112 18 16.43 0.26 0.32 ropean Union standards (4 ppb). However, except
12CS_118 20 10.00 0.3 0.20 12CS_104, all the genotypes have their aflatoxin concen-
12CS_119 20 7.07 0.42 0.28 tration level higher than the Chinese (20 ppb) standards.
International Journal of Agronomy 5

25

20

Number of genotypes

15

10

0
4 ppb≤ Afla 4 ppb < Afla ≤ 20 ppb < Afla ≤ 1000 ppb < 2000 ppb < Afla > 4000 ppb
20 ppb 1000 ppb Afla ≤ 2000 Afla ≤ 4000
ppb ppb
Figure 1: Number of peanut genotypes according to aflatoxin concentration level interval values.

35

30

25
Number of genotypes

20

15

10

0
10% ≤ Inc 10% < Inc ≤ 20% < Inc ≤ 30% < Inc ≤ 40% < Inc ≤ Inc > 50%
20% 30% 40% 50%
Figure 2: Number of peanut genotypes showing aflatoxin presence according to incidence intervals.

Indeed, the highest aflatoxin concentration level was ob-
served with genotype 78-936. The contrasting genotypes
observed in this study can be used as positive and negative
checks, respectively, for accurate field experiment. Fur-
thermore, these contrasted genotypes can be used to develop
mapping population for genetic study such as inheritance of
aflatoxin and identification of quantitative trait loci (QTL).
The varieties 55-437 and 73-30 showed incidence less than
15% as reported by the previous study realized 30 years ago
by Zambettakis et al. [13], but their aflatoxin concentration
levels were largely up to the European Union standards.
The correlation test showed a positive relationship be-
tween A. flavus colonization and aflatoxin contamination.
This confirmed that the presence of A. flavus induced af-
latoxin production in seeds. Hierarchical classification
highlighted three clusters according to incidence, severity,
and aflatoxin concentration levels. The relatively low values
of incidence observed on the 33 genotypes belonged to
cluster 1 should be confirmed under field conditions. These
genotypes can be evaluated in different locations on infested
fields.
5. Conclusion
This study uncovered that the lines 12CS_104 exhibited low
values of incidence and severity. Furthermore, its aflatoxin
6 International Journal of Agronomy

78–936

12CS_031 12CS_028
L27 12CS_076 12CS_011
1 12CS_078 12CS_034 12CS_022 12CS_031 12CS_027
12CS_048 12CS_036 12CS_079 12CS_010 12CS_091
55–33 73–30 12CS_060 12CS_072 12CS_096 12CS_085
12CS_095 12CS_084 12CS_024 12CS_052
12CS_111 12CS_055
12CS_090 12CS_041 12CS_053
0 12CS_033 12CS_008 12CS_063 12CS_075
Dim2 (39.5%)

12CS_039 12CS_047 73–33 12CS_070 12CS_012

12CS_104
12CS_032 12CS_112 12CS_018 12CS_05412CS_066 12CS_051
55–437 12CS_007 GC–8–35
12CS_061 12CS_020 12CS_009 12CS_004 12CS_016
–1 12CS_037 Fleur11 12CS_050
12CS_042
12CS_062 12CS_110
12CS_006
12CS_059 12CS_021

–2 12CS_018
12CS_001
12CS_100

–3

–2 0 2
Dim1 (60.5%)

Group 1
Group 1
Group 1

Figure 3: Principal component analysis biplot showing peanut genotypes clustering based on their severity and incidence.

Table 5: Description of each cluster based on incidence, aflatoxin concentration levels, and paragon and singular genotype per cluster.
Cluster 1 Cluster 2 Cluster 3
Overall † Overall Overall
Mean p value Mean p value Mean p value
mean mean mean
Description of clusters by variables
Incidence 15.09 20.35 <10−3 18.8 20.35 >0.05 35.00 20.35 <10−3
Aflatoxin 915.65 2143.89 <10−3 4075.50 2143.89 <10−3 2279.57 2143.89 >0.05
Description of clusters by distances
Top 3 representative 12CS_039 12CS_090 73-33 12CS_010 12CS_079 12CS_027 12CS_050 12CS_066 12CS_016
genotypes†† (0.11) (0.16) (0.29) (0.12) (0.22) (0.24) (0.15) (0.41) (0.42)
Top 3 characteristic 12CS_104 55-33 12CS_111 78-936 12CS_028 12CS_031 12CS_021 12CS_001 12CS_100
genotypes††† (2.82) (2.75) (2.74) (3.68) (2.39) (2.28) (3.45) (3.00) (2.59)
†
Correlation signification of variables with a cluster. †† Based on the closest distance between each genotype and the respective cluster centres. ††† Based on the
farthest distance from a genotype projected point in a cluster to the centres of the two others.

concentration level was smaller than standards. This ge- Data Availability
notype represents a relevant tool for the breeding pro-
gram for resistance to A. flavus as a potentially resistant The data used to support the findings of this study are
gene donor. available from the corresponding author upon request.
International Journal of Agronomy
Conflicts of Interest
The authors declare no conflicts of interest regarding the
publication of this paper.
Acknowledgments
The authors sincerely thank the West Africa Agricultural
Productivity Program (WAAPP) for financial support and
facilities help.
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